Microbial interactions elicit a range of host plant responses from antagonistic or neutral reactions to beneficial reactions that confer enhanced fitness. The discovery that some rhizobacteria can enhance plant growth after root colonization is one example of a beneficial interaction and these bacteria have been appropriately termed plant growth promoting rhizobacteria (PGPR; Kloepper, J. W. et al., Proc of the 4th Internat. Conf on Plant Pathogenic Bacteria, Station de Pathologie Vegetale et Phytobacteriologie (1978); Lugtenberg, B. et al., Annu Rev Microbiol, 63:541-556 (2009); Nelson, L. M., Plant growth promoting rhizobacteria (PGPR), 10.1094/CM-2004-0301-05-RV (2004). The interaction between PGPR and plants occurs at the root interface where bacterial growth is promoted by root exudates while concomitantly the bacteria enhance plant growth and suppress disease (see van Loon, L., European Journal of Plant Pathology, 119:243-254 (2007) for review). This interaction is associated with immense diversity in the types of PGPR, multiple modes of action by which these microbial associates influence plant growth, and altered metabolic pathways within the plant host.
There are over two dozen genera of rhizobacteria reported to confer biocontrol or plant growth promoting traits to date, with additional genera being discovered (Kim, Y. C. et al., Appl Environ Microb, 77:1548-1555 (2011)). For example, Saikia, R. et al., Curr Microbiol, 62:434-444 (2011) cultured 25 fluorescent pseudomonas from rhizospheric soil of tea plants and found that most of the isolates had strong antagonistic activity against numerous plant fungal pathogens. Multiple mechanisms were found to account for this antagonistic activity, including production of siderophores, salicylic acid (SA), hydrogen cyanide or chitinase (Saikia, R. et al., Curr Microbiol, 62:434-444 (2011)). A similar approach was used to characterize rhizobacteria in wheat fields where 17 isolates from multiple genera were found to promote plant growth through nitrogen-fixation, auxin production or phosphate solubilization (Venieraki, A. et al., Microb Ecol, 61:277-285 (2011)). Another study investigating rhizobacteria from saline soils within wheat fields found evidence of plant growth promotion through auxin, gibberellin or siderophore production as well as phosphorous solubilization (Upadhyay, S. K. et al., Curr Microbiol, 59:489-496 (2009)). Such studies have led to the generalization that rhizobacteria can promote plant growth through multiple modes of action, categorized as nitrogen fixation, ion uptake (especially Fe and P), production of plant hormones and modulation of plant development (e.g., ACC deaminase) (van Loon, L., European Journal of Plant Pathology, 119:243-254 (2007)).
In addition to the indirect effects on plant growth described above, rhizobacteria can promote host growth through direct antagonism to deleterious microorganisms through antibiotic production and competition for nutrients (Handelsman, J. et al., Plant Cell, 8:1855-1869 (1996); van Loon, L., European Journal of Plant Pathology, 119:243-254 (2007)) or by priming the plant for enhanced defense through local and systemic signaling. PGPR-induced systemic defense signaling was elegantly discovered when Pseudomonas bacteria were inoculated into the rhizosphere while the pathogen was inoculated to aerial stems (van Peer, R. et al., Phytopathology 81:728-734 (1991)) and leaves (Gang, W. et al., Phytopathology, 81:1508-1512 (1991)), resulting in an observed reduction in disease severity (reviewed in Bakker, P. A. H. M. et al., Phytopathology, 97:239-243 (2007)). This response has since been termed induced systemic resistance (ISR) and is mediated by a myriad of rhizobacteria and biological control agents in addition to Pseudomonas. Investigations using Arabidopsis mutants found that induction of ISR with P. fluorescens WCS417r was independent of the SA pathway yet required functioning jasmonic acid (JA) and ethylene pathways (Pieterse, C. M. J. et al., Plant Cell, 906 10:1571-1580 (1998); Pieterse, C. M. J. et al., Int S Crop 61:209-220 (1996)). Systemic acquired resistance (SAR) is the other known plant systemic defense pathway and differs from ISR by requiring a functioning SA pathway but is not dependent on JA or ethylene pathways (Durrant, W. E. et al. Annu Rev Phytopathol 42:185-209 (2004), and references therein).
P. fluorescens strain Pf-5 was isolated from the cotton rhizosphere with resynthesis studies demonstrating disease symptom suppression from the widespread pathogens Rhizoctonia solani and Phytium ultimum on cotton, cucumber, pea and maize (Howell, C. R. et al., Phytopathology 69: 480-482 (1979); Kraus, J. et al., Phytopathology 82:264-271 (1992); Loper, J. E. et al., Phytopathology 97:233-238 (2007)). Subsequent studies found that Pf-5 disease suppression was also evident for a myriad of soil-borne pathogens and additional host species such as Pyrenophora tritici-repentis with wheat plants, Sclerotinia homoeocarpa and Drechslera poae with turfgrass (Loper, J. E. et al., Phytopathology 97:233-238 (2007); for review). Due to the wide variety of disease suppression and broad host specificity, Pf-5 has become a common reference strain in biological control studies. In addition, the genome sequence of Pf-5 is complete (Paulsen, I. T. et al., Biotechnol 23:873-878 (2005)) making this an ideal reference strain for studies incorporating molecular genetic scales.
Despite considerable advances in the understanding of PGPR-mediated host plant systemic defense, there are relatively few studies that place such results within a global-view that links defense pathways to consequences on core metabolism and physiology, e.g., transcriptomic studies investigating the colonization of P. fluorescens WCS417r to Arabidopsis (Verhagen, B. W. M. et al. Molecular Plant-Microbe Interactions 17:895-908 (2004)), Bradyrhizobium sp. strain ORS278 with Arabidopsis (Cartieaux, F. et al., Molecular Plant-Microbe Interactions 21:244-259 (2008)) and P. fluorescens FPT9601-T5 with Arabidopsis (Wang, Y. et al., Molecular Plant-Microbe Interactions 18:385-396 (2005)). Similarly, few studies have looked at the consequences of PGPR on host plant physiology (e.g., photoprotective mechanisms; Bashan, Y. et al., Can J Microbiol 50:521-577 (2004)) or comprehensive metabolic profiles (Walker, V. et al., New Phytologist 189:494-506 (2011)). Therefore, insight into the conservation or diversification of host plant responses to PGPR inoculation is limited. Integration of multi-omics data offers an opportunity by which the consequences of PGPR inoculation on plant physiology and multi-organ signaling can be dissected.